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Evaluation of surveillance methods for Staphylococcal toxic shock syndrome.

Staphylococcal staphylococcal

pertaining to Staphylococcus spp.

staphylococcal clumping test
used as a means of measuring the quantity of fibrinogen-split products in a sample of blood.
 toxic shock syndrome toxic shock syndrome (TSS). acute, sometimes fatal, disease characterized by high fever, nausea, diarrhea, lethargy, blotchy rash, and sudden drop in blood pressure. It is caused by Staphylococcus aureus, an exotoxin-producing bacteria (see toxin).  (TSS See ITU. ) is a severe illness associated with toxin-producing Staphylococcus aureus Staphylococcus au·re·us
A bacterium that causes furunculosis, pyemia, osteomyelitis, suppuration of wounds, and food poisoning.

Staphylococcus aureus Staphylococcus pyogenes
. First named in 1978, TSS has been associated with tampon tampon /tam·pon/ (tam´pon) [Fr.] a pack, pad, or plug made of cotton, sponge, or other material, variously used in surgery to plug the nose, vagina, etc., for the control of hemorrhage or the absorption of secretions.  use, intravaginal contraceptive devices, and skin infections, particularly after surgical procedures Surgical procedures have long and possibly daunting names. The meaning of many surgical procedure names can often be understood if the name is broken into parts. For example in splenectomy, "ectomy" is a suffix meaning the removal of a part of the body. "Splene-" means spleen.  (1,2). In January 1980, the Minnesota Department of Health (MDH MDH Minnesota Department of Health
MDH Mälardalens Högskola (Swedish)
MDH Malate Dehydrogenase
MDH Manila Doctors' Hospital
MDH Carbondale, IL, USA - Southern Illinois Airport (Airport Code) 
) initiated surveillance for TSS with active and passive components. The national incidence of TSS decreased during 1980-1996 (3,4) after removal of high-absorbency tampons from the market and public awareness campaigns. In subsequent years, surveillance methods in Minnesota were changed to a solely passive surveillance system that relied on clinicians to report cases. MDH uses the 1997 case definition of the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center.  (CDC See Control Data, century date change and Back Orifice.

CDC - Control Data Corporation
) (Atlanta, GA, USA) to determine case criteria for any probable TSS case ([greater than or equal to]4 clinical criteria and laboratory criteria) considered reportable (Table 1) (5). Given the complexity of the case definition, we suspected that TSS underreporting was likely.

Recently, several factors, including increasing prevalence of community-associated methicillin-resistant S. aureus The aureus (pl. aurei) was a gold coin of ancient Rome valued at 25 silver denarii. The aureus was regularly issued from the 1st century BC to the beginning of the 4th century AD, when it was replaced by the solidus.  that carries superantigens and the trend toward earlier menarche menarche /me·nar·che/ (me-nahr´ke) establishment or beginning of the menstrual function.menar´cheal

The first menstrual period, usually during puberty.
, suggested that the incidence of TSS might be increasing (6,7). Additionally, the number of requests for superantigen testing in the Minneapolis--St. Paul (MSP (1) (Management Service Provider or Managed Service Provider) An organization that manages a customer's computer systems and networks which are either located on the customer's premises or at a third-party datacenter. ) area made to a reference microbiology laboratory that tests staphylococcal isolates from TSS cases increased during 2000-2003 (8). To determine the incidence of TSS, active surveillance was initiated at all MSP area hospitals using International Classification of Diseases, 9th Revision (ICD-9), codes assigned at hospital discharge. We compared passive surveillance reports with ICD-9 codes The following is a list of codes for International Statistical Classification of Diseases and Related Health Problems. These codes are in the public domain.
See also
 to determine an effective and efficient surveillance method for TSS.

The Study

The MSP area is composed of 7 counties with a population of 2,642,056 (2000 US Census) and 24 acute-care hospitals. Requests were sent to medical record departments of these hospitals for data on inpatients discharged from hospitals from January 1, 2000, through December 31, 2003, whose medical records indicated [greater than or equal to]1 of the select ICD-9 study codes. Medical records from all hospitalizations receiving the TSS-specific code (040.82 or 040.89) were reviewed (Figure), and a 20% random sample of medical records from hospitalizations that received [greater than or equal to]1 nonspecific nonspecific /non·spe·cif·ic/ (non?spi-sif´ik)
1. not due to any single known cause.

2. not directed against a particular agent, but rather having a general effect.


 TSS study code (Table 2) from within each hospital was reviewed. Each medical record was reviewed for TSS case criteria and pertinent epidemiologic and clinical information. Additionally, death certificates assigned the ICD-10 code for TSS (A48.3) and cases from the Minnesota Unexplained Critical Illness and Death of Possible Infectious Etiology project (UNEX UNEX University-Class Explorer (NASA)
UNEX University Explorer
) (9) during 2000-2003 were reviewed. TSS cases identified through ICD-9 code searches were compared with cases reported to MDH during 2000-2003. Data were analyzed with Stata version 9 (StataCorp, College Station, TX, USA). Statistical analyses included Pearson and McNemar [chi square chi square (kī),
n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies.
] tests.

Of 7,414 hospitalizations with [greater than or equal to]1 study code, 116 (1.6%) were assigned the TSS-specific code and were reviewed (Figure). Of the remaining 7,298 hospitalizations assigned [greater than or equal to]1 nonspecific TSS code, 1,575 (21.6%) randomly selected hospitalizations were reviewed. Of these 1,691 hospitalizations, 55 had 5 or 6 criteria for TSS, of which 12 (22%) met the CDC case definition for streptococcal streptococcal /strep·to·coc·cal/ (-kok´al) pertaining to or caused by a streptococcus.
Streptococcal (Streptococcus)
Pertaining to any of the Streptococcus bacteria.
 TSS, and 7 were non-MSP residents. The remaining 36 cases were probable or confirmed TSS. No cases from UNEX or death certificate searches met the TSS case definition. Of the 36 TSS cases, 17 (47%) were reported to MDH by passive surveillance. Thirty-one (86%) cases were found by using TSS-specific ICD-9 codes. Five cases were found by using non-TSS-specific ICD-9 codes. After adjusting for 20% random sampling for cases identified by non-TSS-specific codes, we identified the estimated number of cases by using non-TSS-specific codes to be 25. This analysis resulted in 56 estimated TSS cases identified in the surveillance area during 2000-2003 by using ICD-9 codes.

The TSS-specific ICD-9 code search identified 31 of the 56 estimated TSS cases (sensitivity 55%, specificity 99%). Seventeen cases were reported to MDH by passive surveillance (sensitivity 30%, specificity 99.9%); all were coded with the TSS-specific code. The TSS-specific ICD-9 code search was more sensitive than passive surveillance (p = 0.0005, McNemar [chi square] 12.25). Of those cases reported to MDH, more were likely to be associated with menstruation menstruation, periodic flow of blood and cells from the lining of the uterus in humans and most other primates, occurring about every 28 days in women. Menstruation commences at puberty (usually between age 10 and 17).  (14/17 vs. 5/19; p<0.001) and to have had a positive test result for S. aureus (16/17 vs. 11/19; p = 0.01). Twenty-seven of 36 TSS cases detected had a bacterial culture positive for S. aureus. The 3 TSS cases with methicillin-resistant S. aureus isolates were not reported to MDH. The positive predictive value Positive predictive value (PPV)
The probability that a person with a positive test result has, or will get, the disease.

Mentioned in: Genetic Testing

positive predictive value 
 of being a case among those coded with the TSS-specific code was 27% (31/116). In 68 of 116 cases that received the TSS-specific code, there was clinical suspicion clinical suspicion A working hypothesis about a Pt's diagnosis, which is then tested with appropriately targeted tests to arrive at a definitive diagnosis; a CS is based on a constellation of findings in a Pt that suggests to the physician a limited palette of  of TSS, but these cases did not meet the clinical case definition (<5 criteria): 10 were streptococcal TSS and 7 were in non-MSP residents. All 17 cases reported to MDH were detected through the ICD-9 code search.



Surveillance for TSS is challenging given the lack of a diagnostic test and a case definition with multiple components. Under the current passive surveillance system, between one third and half of potential TSS cases were identified. Discrepancies were found in reporting, with menstruation-associated cases more likely to be reported to be spoken of; to be mentioned, whether favorably or unfavorably.

See also: Report
 to MDH than nonmenstrual-associated cases. This discrepancy was observed with prior active surveillance efforts (10).

Using ICD-9 codes, we found 12 TSS cases that were of streptococcal etiology. Accuracy may be improved by developing separate ICD-9 codes specific for staphylococcal, streptococcal, or unidentified TSS. In addition to the TSS-specific ICD-9 code, we selected 5 other ICD-9 codes on the basis of previous studies to address the concern that TSS cases may be classified under a staphylococcal infection Staphylococcal infection
An infection caused by any of several pathogenic species of staphylococcus, commonly characterized by the formation of abscesses of the skin or other organs.

Mentioned in: Fracture Repair
 or sepsis Sepsis Definition

Sepsis refers to a bacterial infection in the bloodstream or body tissues. This is a very broad term covering the presence of many types of microscopic disease-causing organisms.
 code, but not the TSS-specific code (8-10). These 5 additional non-TSS-specific ICD-9 codes required reviewing 1,575 medical records; only 5 (0.3%) additional TSS cases were identified. The non-TSS-specific ICD-9 codes detected 25 estimated cases. However, this detection required 8 trained staff and substantial resources with [approximately equal to]40 minutes required per medical record review.

Passive surveillance requires fewer public health resources because it relies on clinicians to report cases. Active surveillance involves public health resources in identifying cases. The disadvantage of passive surveillance is the potential for missed cases. Despite possible inaccuracies associated with the assignment of ICD-9 codes, these codes represent a standardized data source that may be readily available. In the absence of a specific diagnostic test, ICD-9 codes represent an efficient method for surveillance and following trends.

Medical record abstraction per hospitalization hospitalization /hos·pi·tal·iza·tion/ (hos?pi-t'l-i-za´shun)
1. the placing of a patient in a hospital for treatment.

2. the term of confinement in a hospital.
 was labor- and resource-intensive and is not feasible for most health departments. With increasing use of automated electronic reporting for disease surveillance (11), querying hospital discharge data for the TSS-specific ICD-9 code is a feasible adjunct to passive surveillance to detect TSS trends over time. Consequently, it is imperative that clinicians and coders are thorough to ensure that ICD-9 codes are accurate.

We found it useful to add regular ICD-9 code searches for TSS-specific codes as an active surveillance adjunct to our passive surveillance system. This addition increases sensitivity of TSS surveillance with a minimal increase in resources. Use of this more sensitive system increases the ability to detect trends in TSS, which may develop because of changes in bacterial virulence Virulence

The ability of a microorganism to cause disease. Virulence and pathogenicity are often used interchangeably, but virulence may also be used to indicate the degree of pathogenicity.
 characteristics, host characteristics such as the use of new devices or products, changes in human behavior, or changes in host susceptibility. Evaluation of this approach in other areas to assess sensitivity of TSS surveillance would be useful because coding practices may differ.

DOI (Digital Object Identifier) A method of applying a persistent name to documents, publications and other resources on the Internet rather than using a URL, which can change over time. : 10.3201/eid1505.080826


We thank Brenda Jewel, Craig Morin, Jean Rainbow, and Lori Triden for assistance with data collection; Elly Pretzel for graphics assistance; and Catherine Lexau and Tyson Rogers for statistical assistance.

This study was supported by grants from the National Institutes of Health (Ruth L. Kirschstein National Research Service Award T32 AI 055433-2), the Loan Repayment Program, the National Institute of Allergy and Infectious Disease Infectious disease

A pathological condition spread among biological species. Infectious diseases, although varied in their effects, are always associated with viruses, bacteria, fungi, protozoa, multicellular parasites and aberrant proteins known as prions.
 (Extramural extramural /ex·tra·mu·ral/ (-mur´il) situated or occurring outside the wall of an organ or structure.


situated or occurring outside the wall of an organ or structure.
 Clinical Research L30 AI 071582-01), and the Centers for Disease Control and Prevention (Emerging Infections Program CDC 5 R01 CI000209).

Use of trade names is for identification only and does not imply endorsement by the Public Health Service or by the U.S. Department of Health and Human Services Noun 1. Department of Health and Human Services - the United States federal department that administers all federal programs dealing with health and welfare; created in 1979
Health and Human Services, HHS


(1.) Reingold AL, Hargrett NT, Dan BB, Shands KN, Strickland BY, Broome CV. Nonmenstrual toxic shock syndrome: a review of 130 cases. Ann Intern intern /in·tern/ (in´tern) a medical graduate serving in a hospital preparatory to being licensed to practice medicine.

in·tern or in·terne
 Med. 1982;96:871-4.

(2.) Kain KC, Schulzer M, Chow AW. Clinical spectrum of nonmenstrual toxic shock syndrome (TSS): comparison with menstrual TSS by multivariate discriminant dis·crim·i·nant  
An expression used to distinguish or separate other expressions in a quantity or equation.
 analyses. Clin Infect Dis. 1993;16:100-6.

(3.) Gaventa S, Reingold AL, Hightower AW, Broome CV, Schwartz B, Hoppe C, et al. Active surveillance for toxic shock syndrome in the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. , 1986. Rev Infect Dis. 1989;11(Suppl 1):S28-34.

(4.) Hajjeh RA, Reingold A, Weil A, Shutt K, Schuchat A, Perkins BA. Toxic shock syndrome in the United States: surveillance update, 1979-1996. Emerg Infect Dis. 1999;5:807-10.

(5.) Centers for Disease Control and Prevention. Toxic shock syndrome 1997 case definition [cited 2005 Oct 5]. Available from

(6.) McDowell MA, Drody DJ, Hughes JP. Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES NHANES National Health and Nutrition Examination Survey (US CDC) ) 1999-2004. J Adolesc Health. 2007;40:227-31. DOI: 10.1016/j.jadohealth.2006.10.002

(7.) Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sorensen TI, et al. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics. 2008;121:S17291. DOI: 10.1542/peds.2007-1813D

(8.) Schlievert PM, Tripp TJ, Peterson ML. Reemergence of staphylococcal toxic shock syndrome in Minneapolis-St. Paul, Minnesota, during the 2000-2003 surveillance period. J Clin Microbiol. 2004;42:2875-6. DOI: 10.1128/JCM.42.6.2875-2876.2004

(9.) Hajjeh RA, Relman D, Cieslak PR, Sofair AN, Passaro D, Flood J, et al. Surveillance for unexplained deaths and critical illnesses due to possibly infectious causes, United States, 1995-1998. Emerg Infect Dis. 2002;8:145-53.

(10.) Osterholm MT, Forfang JC. Toxic-shock syndrome in Minnesota: results of an active-passive surveillance system. J Infect Dis. 1982;145:458-64.

(11.) Lazarus R, Klompas M, Campion campion: see pink.

Any of the ornamental rock-garden or border plants that make up the genus Silene, of the pink family, consisting of about 500 species of herbaceous plants found throughout the world.
 FX, McNabb SJ, Hou X, Daniel J, et al. Electronic support for public health: validated case finding and reporting of notifiable diseases The following is a list of notifiable diseases arranged by country. Australia
  • Acquired Immunodeficiency Syndrome (AIDS)
  • Anthrax
  • Arbovirus infections:
 using electronic medical data. J Am Med Inform Assoc. 2009;16:18-24. DOI: 10.1197/jamia.[M.SUP.2]848

Lindsey Lesher, Aaron DeVries, Richard Danila, and Ruth Lyn eld

Author affiliations: Minnesota Department of Health, St. Paul St. Paul

as a missionary he fearlessly confronts the “perils of waters, of robbers, in the city, in the wilderness.” [N.T.: II Cor. 11:26]

See : Bravery
, Minnesota, USA (L. Lesher, A. DeVries, R. Danila, R. Lynfield); and University of Minnesota (body, education) University of Minnesota - The home of Gopher.

Address: Minneapolis, Minnesota, USA.
, Minneapolis, Minnesota “Minneapolis” redirects here. For other uses, see Minneapolis (disambiguation).
Minneapolis (pronounced IPA: /ˌmɪniˈæpəlɪs/) is the largest city in the U.S.
, USA (A. DeVries)

Ms Lesher is an epidemiologist in the Emerging Infections Program at the Minnesota Department of Health. Her research interests include epidemiologic methods and disease caused by S. aureus.

Address for correspondence: Lindsey Lesher, Minnesota Department of Health, 625 Robert St N, PO Box 64975, St. Paul, MN 55164-0975, USA; email:
Table 1. Staphylococcal toxic shock syndrome case definitions*

Criteria                         Definition


  Fever                          Temperature [greater than or equal
                                 to]38.9[degrees]C (102.0[degrees]F)

  Rash                           Diffuse macular erythroderma

  Desquamation                   1-2 weeks after onset of illness,
                                 particularly on the palms
                                 and soles

  Hypotension                    Systolic blood pressure [less than
                                 or equal to]90 mm Hg for adults or
                                 <5th percentile by age for
                                 children <16 years of age;
                                 orthostatic decrease in diastloc
                                 blood pressure [greater than or
                                 equal to]5 mm Hg from lying to
                                 sitting, orthostatic syncope,
                                 or orthostatic dizziness

  Multisystem organ involvement

    Gastrointestinal             Vomiting or diarrhea at onset of

    Muscular                     Severe myalgia or creatine
                                 phosphokinase level at least twice
                                 the upper limit of normal

    Mucous membrane              Vaginal, oropharyngeal, or
                                 conjunctival hyperemia

    Renal                        Blood urea nitrogen or creatinine
                                 at least twice the upper limit of
                                 normal for laboratory or urinary
                                 sediment with pyuria ([greater
                                 than or equal to]5 leukocytes by
                                 high-power field) in the absence
                                 of urinary tract infection

    Hepatic                      Total bilirubin, alanine
                                 aminotransferase, or aspartate
                                 aminotransferase levels at least
                                 twice the upper limit of normal

    Hematologic                  Platelet counts [less than or
                                 equal to]100 x [10.sup.9]/L

    Central nervous system       Disorientation or alterations in
                                 consciousness with focal neurologic
                                 signs when fever and
                                 hypotension are absent


  Culture                        If obtained, negative results on
                                 blood, throat, or cerebrospinal
                                 fluid cultures (blood culture may
                                 be positive for Staphylococcus

  Titer                          If obtained, no increase in titer
                                 for Rocky Mountain spotted fever,
                                 leptospirosis, or measles

Case classification

  Probable                       Meets laboratory criteria and in
                                 which 4 of 5 clinical findings
                                 described above are present

  Confirmed                      Meets laboratory criteria and in
                                 which all 5 of the clinical
                                 findings described above are
                                 present, including desquamation,
                                 unless the patient dies before
                                 desquamation occurs

* From the US Centers for Disease Control and Prevention (5).

([dagger]) Involving [greater than or equal to]3 organ systems.

Table 2. ICD-9 study codes used for staphylococcal toxic shock
syndrome case ascertainment *

Code                             Associated diagnosis

Specific toxic shock syndrome

040.89 or 040.82 ([dagger])      Toxic shock syndrome

Nonspecific toxic shock
syndrome codes

038.11                           Staphylococcus aureus septicemia
038.19 ([double dagger])         Other staphylococcal septicemia
038.9                            Unspecified sepsis
785.5                            Shock without mention of trauma
785.59 or 785.52 ([dagger])      Sepsis

* ICD-9, International Classification of Diseases, 9th Revision.

([dagger])The code assigned to toxic shock syndrome changed from
040.89 to 040.82 on October 1, 2002, and the code assigned to
sepsis changed from 785.59 to 785.52 on October 1, 2003. Although
the codes changed, their associated diagnoses remained unchanged
and are considered mutually exclusive.

([double dagger]) Code eliminated after interim analysis of 627
medical records at 14 of 24 hospitals. Of 122 records receiving
only this code, 40% had 0 case criteria, all had [less than or
equal to]3 criteria, and 88% had bacteremia with a staphylococcal
species other than S. aureus.
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Title Annotation:DISPATCHES
Author:Lesher, Lindsey; DeVries, Aaron; Danila, Richard; eld, Ruth Lyn
Publication:Emerging Infectious Diseases
Date:May 1, 2009
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